Published online : 31 May 2022
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AIMSurv: First pan-European harmonized surveillance of Aedes invasive mosquito species of relevance for human vector-borne diseases
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Miguel Ángel Miranda, Carlos Barceló, Daniele Arnoldi, Xenia Augsten, Karin Bakran-Lebl, George Balatsos, Mikel Bengoa, Philippe Bindler, Kristina Boršová, Maria Bourquia, Daniel Bravo-Barriga, Viktória Čabanová, Beniamino Caputo, Maria Christou, Sarah Delacour, Roger Eritja, Ouafaa Fassi-Fihri, Martina Ferraguti, Eleonora Flacio, Eva Frontera, Hans-Peter Fuehrer, Ana L. García-Pérez, Pantelis Georgiades, Sandra Gewehr, Fátima Goiri, Mikel Alexander González, Martin Gschwind, Rafael Gutiérrez-López, Cintia Horváth, Adolfo Ibáñez-Justicia, Viola Jani, Përparim Kadriaj, Katja Kalan, Mihaela Kavran, Ana Klobucar, Kornélia Kurucz, Javier Lucientes, Renke Lühken, Sergio Magallanes, Giovanni Marini, Angeliki F. Martinou, Alice Michelutti, Andrei Daniel Mihalca, Tomás Montalvo, Fabrizio Montarsi, Spiros Mourelatos, Nesade Muja-Bajraktari, Pie Müller, Gregoris Notarides, Hugo Costa Osório, José A. Oteo, Kerem Oter, Igor Pajović, John R. B. Palmer, Suncica Petrinic, Cristian Răileanu, Christian Ries, Elton Rogozi, Ignacio Ruiz-Arrondo, Isis Sanpera-Calbet, Nebojša Sekulić, Kivanc Sevim, Kurtesh Sherifi, Cornelia Silaghi, Manuel Silva, Nikolina Sokolovska, Zoltán Soltész, Tatiana Sulesco, Jana Šušnjar, Steffanie Teekema, Andrea Valsecchi, Marlen Ines Vasquez, Enkelejda Velo, Antonios Michaelakis, William Wint, Dušan Petrić, Francis Schaffner, Alessandra della Torre, Consortium AIM-COST/AIM-Surv , AIMSurv: First pan-European harmonized surveillance of Aedes invasive mosquito species of relevance for human vector-borne diseasesGigabyte, 2022  https://doi.org/10.46471/gigabyte.57

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Gigabyte
Gigabyte
2709-4715
GigaScience Press
Sha Tin, New Territories, Hong Kong SAR
Data description
Background
Vector-borne diseases (VBDs) are caused by a pathogen transmitted by vectors (often an arthropod) between hosts. Emerging or re-emerging VBDs in humans and animals are of increasing concern for public health worldwide [1], particularly mosquito-borne viral diseases such as chikungunya, dengue, West Nile fever and Zika [2, 3].
Some mosquitoes capable of transmitting pathogens are relevant invasive species at the global scale [4, 5]. They are usually introduced into new areas by global trade (for example, used tires, plants) [68] and have spread within Europe through human-assisted pathways favored by environmental and climate change [911].
In Europe, six Aedes invasive mosquito (AIM) species [12, 13] have been introduced since the 1970s: the yellow fever mosquito Aedes (Stegomyia) aegypti (Linnaeus, 1762, NCBI:txid7159); the Asian tiger mosquito, Aedes (Stegomyia) albopictus (Skuse, 1894, NCBI:txid7160); the Japanese bush mosquito Aedes (Hulecoeteomyia) japonicus (Theobald, 1901, NCBI:txid140438); the Korean bush mosquito Aedes (Hulecoeteomyia) koreicus (Edwards, 1917, NCBI:txid586676); the American rock pool mosquito Aedes (Georgecraigius) atropalpus (Coquillett, 1902, NCBI:txid28624) and the American tree-hole mosquito, Aedes (Protomacleaya) triseriatus (Say, 1823, NCBI:txid7162).
Aedes aegypti is a major vector of yellow fever, dengue and chikungunya viruses and is commonly found in tropical and subtropical areas [14]. Recent re-establishment of this species in Europe was recorded on Madeira (Portugal) [15], in parts of southern Russia, Georgia and Turkey [1618], as well as in Fuerteventura (Canary Islands, Spain) [19], from where it was successfully eradicated in 2019. This species has also been detected at several Western European locations such as the Netherlands [20], where it has not established.
The Asian tiger mosquito originates from Southeast Asia and is currently widespread throughout large areas of Africa, Europe, Australia, the Americas, and the Middle East [14, 21]. It is one of the most invasive species in the world, according to the Invasive Species Specialist Group of the International Union for the Conservation of Nature (IUCN) [4]. In Europe, Ae. albopictus was first detected in Albania in 1979 [22]; nowadays this species is found in more than 27 countries. Since 2007, the Asian tiger mosquito has been linked to several outbreaks of arboviral diseases, such as dengue and chikungunya, which were introduced by travelers in different areas of Europe (for example, Italy, France, Croatia, and Spain) [5, 23]. In laboratory trials, Ae. albopictus is a competent vector of more than 26 arboviruses [24]. It is also a nuisance to humans, especially because of its outdoor daylight feeding behavior [25].
Aedes japonicus originates from eastern Asia and is established in North America, Central Europe and areas of southern Europe (such as Spain and Italy) [2628]. It breeds in artificial containers, so its means of introduction and dispersal are like those of Ae. albopictus [27]. Although laboratory trials showed it to be a competent vector of West Nile virus, among others, it is not considered a major vector of VBDs in nature [29].
Aedes koreicus originates from Korea, Japan, and northeast China and is present in some regions of Austria, Belgium, Germany, Hungary, Italy, Slovenia and the Swiss–Italian border [3037]. It is not considered a major vector of VBDs, although field evidence suggests it is a potential vector of Japanese encephalitis virus [38], and laboratory trials have showed low-level transmission of chikungunya and Zika viruses [39, 40]. Moreover, it is likely to be a competent vector of Dirofilaria immitis [41].
Aedes atropalpus is an invasive mosquito species originating from North America, which has been detected in European countries like Italy, France and the Netherlands without any evidence of prolonged establishment [4245]. It is not considered to be a major vector, but in laboratory trials it is a competent vector of viruses such as West Nile [46].
Finally, Aedes triseriatus, which originates from North America, was detected in a single incursion in France in 2004 and was successfully eradicated [44]. La Crosse [47] and West Nile [46] viruses have been detected in field-collected mosquito adults in the USA.
Context
Different EU initiatives exist to map the distribution of invasive mosquitoes. The European Centre for Disease Prevention and Control (ECDC) and the European Food Safety Authority (EFSA) have established VectorNet, a community network for medical entomologists and public health experts. VectorNet produces and periodically updates distribution maps of invasive mosquitoes in Europe [48]. These maps result from the analysis of literature records on the distribution of AIM species in Europe and the contribution of public, academia and research institutions that freely share their data with the VectorNet community. Another initiative is Mosquito Alert [49], a Spanish-originated citizen science campaign to monitor and map Aedes invasive species.
Early detection and surveillance of invasive mosquito species are challenging in terms of coordination and resources. Detection of AIM species may include different means and roles, from national surveillance programs to detect invasive species at points of entry, and to establish early warning rapid response systems to monitor AIM populations. Surveillance is commonly organized at the local and regional levels by public agencies, universities and research institutions [50], leading to different methodologies and strategies for sampling life stages of AIM (eggs, larvae/pupae and adults). Valuable guidelines for conventional surveillance have been produced by the ECDC and the World Health Organization Europe regional Office (EU-WHO) [51]. However, to date, they have never been harmonized and used simultaneously by different entomologist teams across Europe.
To increase harmonization between European entomologists, the Aedes Invasive Mosquito species (AIM) COST Action [52] was initiated in 2018. It had three major objectives: (i) to develop pan-European networking and collaboration in monitoring and surveillance of AIM species; (ii) to increase preparedness and capacity to fight against AIMs by triggering optimization and innovation in AIM control strategies; and (iii) to disseminate, customize and communicate the AIM-COST Action outcomes.
The AIM-COST Action aims to promote data sharing and harmonization. A particularly important objective is to ensure that vector sampling is consistent and compatible throughout Europe to enable an accurate continental picture of vector distributions. For this, AIM-COST organized a training course in Cyprus in January 2020 on harmonizing AIM surveillance across Europe. As a result of this course, trainers and trainees developed a protocol for surveying AIM species that can be applied across Europe. Forty-two teams from 24 countries (23 from Europe and one from North Africa) agreed to participating in the first ever pan-European surveillance of AIMs using a harmonized protocol [53]. The AIMSurv protocol was first implemented in 2020, then extended to 2021 and 2022. The main aim was to provide longitudinal data enabling comparison of seasonality and abundance across Europe and, in a subsequent phase, to compare field data with reports obtained by citizen science (for example, the Mosquito Alert App [54], the data of which has also been published in GBIF [55]). Accordingly, both the presence and absence results of AIMs species were considered equally important to improve the information at the continental level.
Methods
The sampling protocol for pan-European surveillance of AIM species (AIMSurv) harmonized the sampling methods, frequency, minimum length of the sampling period and the form of reporting. A minimum requirements protocol (MRP) was established for different samples (for example, eggs in ovitraps), number of sampled sites, number of traps and frequency of collecting samples. For teams with more resources, a recommended protocol (RP) was also established to either increase the number of samples and/or to sample life stages other than eggs, such as adults.
The use of a common platform for data collection was also suggested: the VECMAP® App system [56] (Avia-GIS, Zoersel, Belgium), which was made freely available by Avia-GIS to all participants during AIMSurv activities.
Minimum requirements protocol
For the MRP, all teams performed the survey in three sampling sites separated by 10 km or more. Five oviposition traps (ovitraps) per site were placed and separated by 15–100 m. The type of ovitrap was selected by each team according to their availability in the region, but usually consisted of 250 to 1000-ml capacity black containers filled with tap water. One scratched wooden tongue depressor (1.7 × 15 cm) per ovitrap was used as a substrate for oviposition. Some teams used similar sized pieces of Masonite board (when part of a pre-existing surveillance network was in place).
The selected sampling sites shared a similar ecology, when possible, in urban and/or suburban areas (e.g., a garden of single-family houses in residential urban/suburban areas, public parks near residential areas, recreational areas). The frequency of sample collection was biweekly over a minimum of 3 months, which included the population peak of the targeted AIM species (e.g., in Spain: from September to November for Ae. albopictus).
The following parameters were recorded: latitude and longitude of the position of each trap; the name of municipality/county/district (according to the country) and locality; start and end date of each trapping event (e.g., a period of 14 days for ovitraps); land use categories (urban, suburban and others); count of each life stage collected (egg and adult), including absences (0 values).
Recommended protocol
The more ambitious RP sampling included additional sampling sites sampled by five ovitraps per site, weekly sampling frequency and sampling length during the whole seasonality of the AIM species including start, peak and end of the mosquito season (e.g., May to November in Central Europe for Ae. albopictus). In addition, sampling adults using one BG-Sentinel™ (Biogents, Germany) trap baited with BG-Lure™ (Biogents, Germany) and/or CO2  per site under a sampling frequency of one trap/night per week was also included. The use of VECMAP® (AVIA-GIS, Belgium) to report the data was also suggested in the RP. Parameters to record were the same as for the MRP, plus the daily or weekly record of meteorological parameters (maximum, minimum, average temperature) per site, collected using data loggers or local weather stations (data not included in the current dataset).
The trap status per trapping event was recorded as follows: ‘Valid’ when the trap (either oviposition or BG-Sentinel) was fully functional during the sampling event; ‘Trap altered’ when oviposition trap was found dry or turned over, or objects or animals, such as snails and lizards, were found inside, but the sample could still be collected. ‘Trap altered’ also referred to BG-Sentinel traps when they were found unplugged or with the battery switched off, or if the funnel was blocked, but the sample could still be collected.
To process samples, eggs of AIM species collected were counted. When needed, for every location a subsample (two out of five ovitrap substrates per locality) of eggs was reared to confirm the species by larva/adult morphology, particularly in areas where several AIM species are present (i.e., Ae. albopictus and Ae. japonicus). Alternatively, when possible and depending on the team’s resources, species were identified using: matrix-assisted laser desorption ionisation–time of flight mass spectrometry (MALDI-TOF MS) or molecular methods (e.g., DNA sequencing).
Adults of AIM species collected in BG-Sentinel™ traps were identified by morphology, and sexed and counted. Suggested identification keys were ECDC (2012) [51] and MosKeyTool V2.1 [57]. Samples of adults were preserved in 96% ethanol and/or cold preserved at −20∕−80 °C to confirm identification if needed (e.g., via molecular tools).
Data validation and quality control
All participants in AIMSurv reported data using a harmonized template. All data reported has been curated and the terminology has been homogenized. Data has been validated using the validator available at the Global Biodiversity Information Facility (GBIF) [58].
Reuse potential
Records presented here represent the first pan-European data on field surveillance of AIM species conducted with harmoniously methodologies and time scales across 24 countries. The records allow the accurate comparison of AIM surveillance, abundance, and seasonality between countries and/or regions. Data can also be compared with other sampling strategies of AIM species, such as citizen science.
Data Availability
The data supporting this article are published through the Universitat de les Illes Balears IPT and are available under a CC0 waiver from GBIF [58]. We kindly ask users to give appropriate credit and attribution if you use this data.
Editor’s note
This paper is part of a series of Data Release articles working with GBIF and supported by the Special Programme for Research and Training in Tropical Diseases (TDR), hosted at the World Health Organization [59].
Declarations
List of abbreviations
AIM: Aedes invasive mosquito; COST: European Cooperation in Science and Technology; ECDC: European Centre for Disease Control; EFSA: European Food Safety Authority; EU: European Union; EU-WHO: World Health Organization Europe regional office; IUCN: International Union for the Conservation of Nature; MALDI-TOF MS: matrix-assisted laser desorption ionization–time of flight mass spectrometry; MRP: minimum requirements protocol; RP: recommended protocol; VBD: vector-borne disease
Ethical approval
Not applicable.
Consent for publication
Not applicable.
Competing Interests
The authors declare that they have no competing interests.
Funding
This study was funded by the Autonomous Province of Trento (Italy) under the project ‘Coordinated surveillance actions on invasive alien species and emerging vector borne diseases’; the City Health Office of the City of Zagreb, within the ‘Program for monitoring invasive mosquito species in the area of the City of Zagreb in 2020’; the Consejería de Economía e Infraestructura of the Junta de Extremadura and the European Regional Development Fund, a Way to Make Europe, through the research project IB16135; Dirección de Salud Pública (Gobierno Vasco), Project EU-LIFE 18 IPC/ES/000001 (Urban Klima 2050) y Programa Estatal de Vigilancia de mosquitos en puertos y Aeropuertos, del Ministerio de Sanidad (Gobierno de España); EMME-CARE project, which has been funded from the European Union’s Horizon 2020 Research and Innovation Programme (grant agreement ID 856612); Institute of Zoology under the project EVOLANTER (project no. 20.80009.7007.02). RL is funded by the Federal Ministry of Education and Research of Germany (BMBF) under the project NEED (grant no. 01Kl2022); LIFE CONOPS project (LIFE12 ENV/GR/000466), funded by the European Commission in the framework of the program LIFE + Environment Policy and Governance; Municipalities of Slovenia: City Municipality of Nova Gorica, City Municipality of Koper, Municipality of Izola, Municipality of Piran and Municipality of Ankaran; National Research, Development and Innovation Office (NKFIH grant numbers KH-130379, PD-135143, FK-138563 and K-135841). The research activity of KK was supported by the Janos Bolyai Research Scholarship of the Hungarian Academy of Sciences and by the ÚNKP-20-5-PTE-597 New National Excellence Program of the Ministry for Innovation and Technology; Portuguese National Program for Vector Surveillance (REVIVE) and we are particularly grateful to the regional workgroup of Algarve for the monitoring activities; PR (19_ECO_0070) project ‘Aves y Enfermedades Infecciosas Emergentes: Impacto de las Especies Exóticas y Migratorias en la transmisión de Malaria aviar y el virus del Nilo Occidental – AvEIEs’ from ‘Ayudas Fundación BBVA a Equipos de Investigación Científica 2019’; project grant number 57 PCCDI/2018, grant agency ‘The Executive Unit for Financing Higher Education, Research, Development and Innovation’ (UEFISCDI) Romania, ‘Collegium Talentum Programme’ of Hungary, Eötvös Loránd University’s ‘Homeland higher education study grant’; Slovak Research Agency VEGA nr. 2/0140/21; Vector Control Needs Assessment in Cyprus, contracted by the World Health Organization (reference 2020/1040069-0); Veneto and Friuli Venezia Giulia Regions (Regional Prevention Plans ‘Entomological Surveillance of vector-borne diseases’ in the Veneto and Friuli Venezia Giulia Regions); the Institute of Public Health, Albania under the program of mosquitoes control in urban and coastal areas.
Authors’ contributions
MAM and AdT conceived this work; MAM, AM, WW, DP and FS designed this work; CB, DA, XA, KB-L, GB, MB, PB, KB, MB, DB-B, VČ, BC, MC, SD, RE, OF-F, MF, EF, EMF-C, HPF, ALG-P, PG, SG, FG, MAG, MG, RG-L, CH, AI-J, VJ, PK, KK, MK, AK, KK, JL, RL, SM, GM, AFM, AM, AM, TM, FM, SM, NM-B, PM, GN, HCO, JAO, KO, IP, JRBP, SP, CR, CR, ER, IR-A, IS-C, NS, KS, KS, CS, MS, NiS, ZS, TS, JŠ, ST, AV, MIV, EV, AM, DP, FS collected the samples and reported results; MAM wrote the original draft and coordinated AIMSurv data compilation and curation; AdT coordinated AIM-COST Action. All authors read, revised, and approved the final manuscript.
Acknowledgements
We acknowledge the support provided by Katia Cezón (GBIF-Spain) in adapting our dataset to the GBIF standards. The work was done within the framework of AIM-COST Action (CA17108).
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Details of collaborative authors
List of authors in Consortium AIM-COST/AIM-Surv